Eph receptor tyrosine kinases in cancer stem cells

Cytokine and Growth Factor Reviews

Volumn 26, Issue 1, 2015, Pages 1-6

  Chen, Jin ^a,b,c,d   Song, Wenqiang ^a,b   Amato, Katherine ^c  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b Division of Rheumatology and Immunology   (United States)

^c Department of Cancer Biology ^*  (United States)

^d VANDERBILT INGRAM CANCER CENTER   (United States)

Author keywords

Cancer stem cells; Eph RTK; Ephrin

Indexed keywords

ALW II 4217; DOXAZOSIN; EPHRIN; EPHRIN RECEPTOR; EPHRIN RECEPTOR A2; EPHRIN RECEPTOR A3; EPHRIN RECEPTOR A4; EPHRIN RECEPTOR B2; EPHRIN RECEPTOR B3; EPHRIN RECEPTOR B4; EPHRIN RECEPTOR TYROSINE KINASE; LITHOCHOLIC ACID; NG 25; NVP BHG 712; PROTEIN KINASE INHIBITOR; PROTEIN TYROSINE KINASE; SALICYLIC ACID DERIVATIVE; UNCLASSIFIED DRUG; UVOMORULIN;

ADULT STEM CELL; ANTINEOPLASTIC ACTIVITY; CANCER INHIBITION; CANCER STEM CELL; CARCINOGENESIS; CARCINOGENICITY; CELL PROLIFERATION; CELL RENEWAL; DRUG TARGETING; HUMAN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; SHORT SURVEY; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL DIVISION; HOMEOSTASIS; METABOLISM; MOLECULARLY TARGETED THERAPY; MOUSE; NEOPLASMS; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIVISION; EPHRINS; HOMEOSTASIS; HUMANS; MICE; MOLECULAR TARGETED THERAPY; NEOPLASMS; NEOPLASTIC STEM CELLS; RECEPTORS, EPH FAMILY; SIGNAL TRANSDUCTION;

EID: 84923043793     PISSN: 13596101     EISSN: 18790305     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2014.05.001     Document Type: Short Survey

References (65)

1. Kreso A., Dick J.E. Evolution of the cancer stem cell model. Cell Stem Cell 2014, 14:275-291.
2. Gilbertson R.J., Graham T.A. Cancer: resolving the stem-cell debate. Nature 2012, 488:462-463.
3. Pasquale E.B. Eph receptors and ephrins in cancer: bidirectional signaling and beyond. Nat Rev Cancer 2010, 10:165-180.
4. Chen J. Regulation of tumor initiation and metastatic progression by Eph receptor tyrosine kinases. Adv Cancer Res 2012, 114:1-20.
5. Chen H., Ma J., Li W., Eliseenkova A.V., Xu C., Neubert T.A., et al. A molecular brake in the kinase hinge region regulates the activity of receptor tyrosine kinases. Mol Cell 2007, 27:717-730.
6. Zhang J., Yang P.L., Gray N.S. Targeting cancer with small molecule kinase inhibitors. Nat Rev Cancer 2009, 9:28-39.
7. Falivelli G., Lisabeth E.M., Rubio de la Torre E., Perez-Tenorio G., Tosato G., Salvucci O., et al. Attenuation of eph receptor kinase activation in cancer cells by coexpressed ephrin ligands. PLoS One 2013, 8:e81445.
8. Carvalho R.F., Beutler M., Marler K.J., Knoll B., Becker-Barroso E., Heintzmann R., et al. Silencing of EphA3 through a cis interaction with ephrinA5. Nat Neurosci 2006, 9:322-330.
9. Yin Y., Yamashita Y., Noda H., Okafuji T., Go M.J., Tanaka H. EphA receptor tyrosine kinases interact with co-expressed ephrin-A ligands in cis. Neurosci Res 2004, 48:285-296.
10. Kao T.J., Kania A. Ephrin-mediated cis-attenuation of Eph receptor signaling is essential for spinal motor axon guidance. Neuron 2011, 71:76-91.
11. Marquardt T., Shirasaki R., Ghosh S., Andrews S.E., Carter N., Hunter T., et al. Coexpressed EphA receptors and ephrin-A ligands mediate opposing actions on growth cone navigation from distinct membrane domains. Cell 2005, 121:127-139.
12. Brantley-Sieders D.M., Zhuang G., Hicks D., Fang W.B., Hwang Y., Cates J.M., et al. The receptor tyrosine kinase EphA2 promotes mammary adenocarcinoma tumorigenesis and metastatic progression in mice by amplifying ErbB2 signaling. J Clin Invest 2008, 118:64-78.
13. Larsen A.B., Pedersen M.W., Stockhausen M.T., Grandal M.V., van Deurs B., Poulsen H.S. Activation of the EGFR gene target EphA2 inhibits epidermal growth factor-induced cancer cell motility. Mol Cancer Res 2007, 5:283-293.
14. Miao H., Li D.Q., Mukherjee A., Guo H., Petty A., Cutter J., et al. EphA2 mediates ligand-dependent inhibition and ligand-independent promotion of cell migration and invasion via a reciprocal regulatory loop with Akt. Cancer Cell 2009, 16:9-20.
15. Pasquale E.B. Eph-ephrin bidirectional signaling in physiology and disease. Cell 2008, 133:38-52.
16. Chen J., Nachebeh A., Scherer C., Ganju P., Reith A., Bronson R., et al. Germline inactivation of the murine Eck receptor tyrosine kinase by retroviral insertion. Oncogene 1996, 12:979-988.
17. Orsulic S., Kemler R. Expression of Eph receptors and ephrins is differentially regulated by E-cadherin. J Cell Sci 2000, 113(Pt 10):1793-1802.
18. Genander M., Halford M.M., Xu N.J., Eriksson M., Yu Z., Qiu Z., et al. Dissociation of EphB2 signaling pathways mediating progenitor cell proliferation and tumor suppression. Cell 2009, 139:679-692.
19. Conover J.C., Doetsch F., Garcia-Verdugo J.M., Gale N.W., Yancopoulos G.D., Alvarez-Buylla A. Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nat Neurosci 2000, 3:1091-1097.
20. Holmberg J., Armulik A., Senti K.A., Edoff K., Spalding K., Momma S., et al. Ephrin-A2 reverse signaling negatively regulates neural progenitor proliferation and neurogenesis. Genes Dev 2005, 19:462-471.
21. Chumley M.J., Catchpole T., Silvany R.E., Kernie S.G., Henkemeyer M. EphB receptors regulate stem/progenitor cell proliferation, migration, and polarity during hippocampal neurogenesis. J Neurosci 2007, 27:13481-13490.
22. Nomura T., Goritz C., Catchpole T., Henkemeyer M., Frisen J. EphB signaling controls lineage plasticity of adult neural stem cell niche cells. Cell Stem Cell 2010, 7:730-743.
23. Hara Y., Nomura T., Yoshizaki K., Frisen J., Osumi N. Impaired hippocampal neurogenesis and vascular formation in ephrin-A5-deficient mice. Stem Cells 2010, 28:974-983.
24. Barker N., van Es J.H., Kuipers J., Kujala P., van den Born M., Cozijnsen M., et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449:1003-1007.
25. Batlle E., Henderson J.T., Beghtel H., van den Born M.M., Sancho E., Huls G., et al. Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 2002, 111:251-263.
26. Genander M., Holmberg J., Frisén J. Ephrins negatively regulate cell proliferation in the epidermis and hair follicle. Stem Cells 2010, 28:1196-1205.
27. Matsuo K., Otaki N. Bone cell interactions through Eph/ephrin: bone modeling, remodeling and associated diseases. Cell Adh Migr 2012, 6:148-156.
28. Irie N., Takada Y., Watanabe Y., Matsuzaki Y., Naruse C., Asano M., et al. Bidirectional signaling through ephrinA2-EphA2 enhances osteoclastogenesis and suppresses osteoblastogenesis. J Biol Chem 2009, 284:14637-14644.
29. Zhao C., Irie N., Takada Y., Shimoda K., Miyamoto T., Nishiwaki T., et al. Bidirectional ephrinB2-EphB4 signaling controls bone homeostasis. Cell Metab 2006, 4:111-121.
30. Goichberg P., Bai Y., D'Amario D., Ferreira-Martins J., Fiorini C., Zheng H., et al. The ephrin A1-EphA2 system promotes cardiac stem cell migration after infarction. Circ Res 2011, 108:1071-1083.
31. Brantley-Sieders D.M. Clinical relevance of Ephs and ephrins in cancer: lessons from breast, colorectal, and lung cancer profiling. Semin Cell Dev Biol 2012, 23:102-108.
32. Brantley-Sieders D.M., Jiang A., Sarma K., Badu-Nkansah A., Walter D.L., Shyr Y., et al. Eph/ephrin profiling in human breast cancer reveals significant associations between expression level and clinical outcome. PLoS ONE 2011, 6:e24426.
33. Zhuang G., Brantley-Sieders D., Vaught D., Yu J., Xie L., Wells S., et al. Elevation of receptor tyrosine kinase EphA2 mediates resistance to trastuzumab therapy. Cancer Res 2010, 70:299-308.
34. Brannan J.M., Dong W., Prudkin L., Behrens C., Lotan R., Bekele B.N., et al. Expression of the receptor tyrosine kinase EphA2 is increased in smokers and predicts poor survival in non-small cell lung cancer. Clin Cancer Res 2009, 15:4423-4430.
35. Faoro L., Singleton P.A., Cervantes G.M., Lennon F.E., Choong N.W., Kanteti R., et al. EphA2 mutation in lung squamous cell carcinoma promotes increased cell survival, cell invasion, focal adhesions, and mTOR activation. J Biol Chem 2010, 285:18575-18585.
36. Kinch M.S., Moore M.B., Harpole D.H.J. Predictive value of the EphA2 receptor tyrosine kinase in lung cancer recurrence and survival. Clin Cancer Res 2003, 9:613-618.
37. Liu F., Park P.J., Lai W., Maher E., Chakravarti A., Durso L., et al. A genome-wide screen reveals functional gene clusters in the cancer genome and identifies EphA2 as a mitogen in glioblastoma. Cancer Res 2006, 66:10815-10823.
38. Wykosky J., Gibo D.M., Stanton C., Debinski W. EphA2 as a novel molecular marker and target in glioblastoma multiforme. Mol Cancer Res 2005, 3:541-551.
39. Landen C.N., Kinch M.S., Sood A.K. EphA2 as a target for ovarian cancer therapy. Expert Opin Ther Targets 2005, 9:1179-1187.
40. Udayakumar D., Zhang G., Ji Z., Njauw C.N., Mroz P., Tsao H. EphA2 is a critical oncogene in melanoma. Oncogene 2011, 30:4921-4929.
41. Zhuang G., Song W., Amato K., Hwang Y., Lee K., Boothby M., et al. Effects of cancer-associated EphA3 mutations on lung cancer. JNCI 2012, 104:1182-1197.
42. Lisabeth E.M., Fernandez C., Pasquale E.B. Cancer somatic mutations disrupt functions of the EphA3 receptor tyrosine kinase through multiple mechanisms. Biochemistry 2012, 51:1464-1475.
43. Bindasend E., Visioli A., Giani F., Lamorte G., Copetti M., Pitter K.L., et al. The EphA2 receptor drives self-renewal and tumorigenicity in stem-like tumor-propagating cells from human glioblastomas. Cancer Cell 2012, 22:765-780.
44. Day B.W., Stringer B.W., Al-Ejeh F., Ting M.J., Wilson J., Ensbey K.S., et al. EphA3 maintains tumorigenicity and is a therapeutic target in glioblastoma multiforme. Cancer Cell 2013, 23:238-248.
45. Aoki M., Yamashita T., Tohyama M. EphA receptors direct the differentiation of mammalian neural precursor cells through a mitogen-activated protein kinase-dependent pathway. J Biol Chem 2004, 279:32643-32650.
46. Miao H., Gale N.W., Guo H., Qian J., Petty A., Kaspar J., et al. EphA2 promotes infiltrative invasion of glioma stem cells in vivo through cross-talk with Akt and regulates stem cell properties. Oncogene 2014.
47. Taddei M.L., Giannoni E., Morandi A., Ippolito L., Ramazzotti M., Callari M., et al. Mesenchymal to amoeboid transition is associated with stem-like features of melanoma cells. Cell Commun Signal 2014, 12:24.
48. Song W., Ma Y., Wang J., Brantley-Sieders D., Chen J. JNK signaling mediates EPHA2-dependent tumor cell proliferation, motility, and cancer stem cell-like properties in non-small cell lung cancer. Cancer Res 2014, 74:2444-2454.
49. Jiao X., Katiyar S., Willmarth N.E., Liu M., Ma X., Flomenberg N., et al. c-Jun induces mammary epithelial cellular invasion and breast cancer stem cell expansion. J Biol Chem 2010, 285:8218-8226.
50. Yoon C.H., Kim M.J., Kim R.K., Lim E.J., Choi K.S., An S., et al. c-Jun N-terminal kinase has a pivotal role in the maintenance of self-renewal and tumorigenicity in glioma stem-like cells. Oncogene 2012, 31:4655-4666.
51. Chen F. JNK-induced apoptosis, compensatory growth, and cancer stem cells. Cancer Res 2012, 72:379-386.
52. Batlle E., Bacani J., Begthel H., Jonkeer S., Gregorieff A., van de Born M., et al. EphB receptor activity suppresses colorectal cancer progression. Nature 2005, 435:1126-1130.
53. Davalos V., Dopeso H., Castano J., Wilson A.J., Vilardell F., Romero-Gimenez J., et al. EPHB4 and survival of colorectal cancer patients. Cancer Res 2006, 66:8943-8948.
54. Guo D.L., Zhang J., Yuen S.T., Tsui W.Y., Chan A.S., Ho C., et al. Reduced expression of EphB2 that parallels invasion and metastasis in colorectal tumours. Carcinogenesis 2006, 27:454-464.
55. Zantek N.D., Azimi M., Fedor-Chaiken M., Wang B., Brackenbury R., Kinch M.S. E-cadherin regulates the function of the EphA2 receptor tyrosine kinase. Cell Growth Differ 1999, 10:629-638.
56. Fang W.B., Brantley-Sieders D.M., Parker M.A., Reith A.D., Chen J. A kinase-dependent role for EphA2 receptor in promoting tumor growth and metastasis. Oncogene 2005, 24:7859-7868.
57. Amato K.R., Wang S., Hastings A.K., Youngblood V.M., Santapuram P.R., Chen H., et al. Genetic and pharmacologic inhibition of EPHA2 promotes apoptosis in NSCLC. J Clin Invest 2014, 124:2037-2049.
58. Noberini R., Lamberto I., Pasquale E.B. Targeting Eph receptors with peptides and small molecules: progress and challenges. Semin Cell Dev Biol 2012, 23:51-57.
59. Liu Y., Gray N.S. Rational design of inhibitors that bind to inactive kinase conformations. Nat Chem Biol 2006, 2:358-364.
60. Choi Y., Syeda F., Walker J.R., Finerty P.J., Cuerrier D., Wojciechowski A., et al. Discovery and structural analysis of Eph receptor tyrosine kinase inhibitors. Bioorg Med Chem Lett 2009, 19:4467-4470.
61. Martiny-Baron G., Holzer P., Billy E., Schnell C., Brueggen J., Ferretti M., et al. The small molecule specific EphB4 kinase inhibitor NVP-BHG712 inhibits VEGF driven angiogenesis. Angiogenesis 2010, 13:259-267.
62. Noberini R., Koolpe M., Peddibhotla S., Dahl R., Su Y., Cosford N.D., et al. Small molecules can selectively inhibit ephrin binding to the EphA4 and EphA2 receptors. J Biol Chem 2008, 283:29461-29472.
63. Noberini R., De S.K., Zhang Z., Wu B., Raveendra-Panickar D., Chen V., et al. A disalicylic acid-furanyl derivative inhibits ephrin binding to a subset of Eph receptors. Chem Biol Drug Des 2011, 78:667-678.
64. Giorgio C., Hassan Mohamed I., Flammini L., Barocelli E., Incerti M., Lodola A., et al. Lithocholic acid is an Eph-ephrin ligand interfering with Eph-kinase activation. PLoS One 2011, 6:e18128.
65. Petty A., Myshkin E., Qin H., Guo H., Miao H., Tochtrop G.P., et al. A small molecule agonist of EphA2 receptor tyrosine kinase inhibits tumor cell migration in vitro and prostate cancer metastasis in vivo. PLoS ONE 2012, 7:e42120.